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There is a story behind every paper. Sometimes it is obvious and sometimes not. In the case we were looking for something else and the discovery of a new DMSP lyase was completely unanticipated. Years before in my lab Jim Tripp had studied Pelagibacter sulfur metabolism because he had found that DMSP allowed cells to grow to higher numbers. We were looking for a magic compound – something that could be added to seawater to stimulate growth.Why was this so important? Well, growth factors are an interesting issue on their own merit but the practical motivation was that we needed the cells to grow better if we were to continue studying them. Jim found that Pelagibacter couldn’t assimilate sulfate to meet its sulfur requirement because of missing genes, and DMSP supplied them with essential sulfur. The study of Pelagibacter would have stalled without that information.

Skip forward. We had reported that sulfate assimilation was incomplete, but we knew that some common genes for sulfur metabolism were present and often expressed. What were these proteins doing? Williams and colleagues had postulated a function for AprAB in the oxidation of the S found in taurine. In hindsight, they are probably right. But, Jing Sun and I speculated that the cells might be using AprAB to oxidize some of the excess S from DMSP. We have colleagues in the Food Science and Technology Department – Yanping and Michael Qian – who are experts at measuring low molecular weight sulfur-containing compounds because they are important in food – notably beer. OSU has a world- class program for training fermentation specialists. So, with Yan Ping and Michael, we did an experiment to track the fate of DMSP sulfur. Of course we measured DMS to help complete the accounting, although we expected that none would be produced because the genome had no annotated DMSP lyase.

We were quite amazed when the cultures produced DMS in substantial amounts.Obviously a DMSP lyase lay hidden in the genome, undetected.Being outsiders in the DMSP field, we turned to a colleague, Andy Johnston, for help. The paper relates how Andy, Jon Todd, and others in his lab found a new lyase enzyme in the genome.

There is a lot more to the story. The Pelagibacter genes for DMSP use are “on” all the time, and apparently not controlled by a switch that turns the genes on and off.Much of our field is concerned with how gene expression is regulated, because new sequencing technologies are very good at measuring this. But, we looked carefully for gene regulation, and saw no evidence for it. To explain the data we proposed that the cells are using kinetic regulation to route sulfur through competing pathways. This fits a model, built up over years, of minimalist gene regulation in Pelagibacter.

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Since Steve has kindly credited me with pioneering work on reduced sulfur compounds in SAR11, particularly DMSP, I think it only fair to say what prompted me to do so. As a struggling grad student, I found myself unable to perform complete metabolic reconstructions for glycolysis and sulfate reduction in the newly acquired genome of the SAR11 representative called HTCC1062. At the same time, I found it curious that I had no trouble with any other essential pathways, and that there were a surprising number of methylases in this exceptionally small genome with very few redundancies. One day Steve asked me to repeat the apparent oddities in the genome so that we could consider the implications in the event that they were real. He asked what the ideal nutrient would be for SAR11. I responded, "It would have less than six carbons, contain reduced sulfur, and might be methylated." Steve closed his eyes and repeated it back to me. He paused, and asked: "Do you know what compound you just described?" I said, "I have no idea." He said, "DMSP. I have friend at WHOI, John Dacey, who makes it. If I ask him for some, will you feed it to SAR11?" I said of course. Eventually, we were able to see that the reduced sulfur was probably the most valuable part of DMSP. I can take credit for hours of BLASTing ORFs and augmenting KEGG charts in Microsoft paintbrush, but the insight that these signs pointed to DMSP belongs to Steve alone. I was fortunate to have the opportunity to provide him with what he needed in order to make this breakthrough. He has a remarkable grasp of marine microbiology, from the global to the cellular scales.

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